Abstract

Interactions among genes and the environment are a common source of phenotypic variation. To characterize the interplay between genetics and the environment at single nucleotide resolution, we quantified the genetic and environmental interactions of four quantitative trait nucleotides (QTN) that govern yeast sporulation efficiency. We first constructed a panel of strains that together carry all 32 possible combinations of the 4 QTN genotypes in 2 distinct genetic backgrounds. We then measured the sporulation efficiencies of these 32 strains across 8 controlled environments. This dataset shows that variation in sporulation efficiency is shaped largely by genetic and environmental interactions. We find clear examples of QTN:environment, QTN: background, and environment:background interactions. However, we find no QTN:QTN interactions that occur consistently across the entire dataset. Instead, interactions between QTN only occur under specific combinations of environment and genetic background. Thus, what might appear to be a QTN:QTN interaction in one background and environment becomes a more complex QTN:QTN:environment:background interaction when we consider the entire dataset as a whole. As a result, the phenotypic impact of a set of QTN alleles cannot be predicted from genotype alone. Our results instead demonstrate that the effects of QTN and their interactions are inextricably linked both to genetic background and to environmental variation.

Highlights

  • As we identify more genetic loci that underlie complex traits, the challenge remains to understand and predict the effects of the causal genetic variants upon individuals’ phenotypes

  • Our quantitative trait nucleotides (QTN) all affect the proportion of cells in a culture that initiate meiosis after a shift from glucose to acetate media

  • The relationship between an allele and the phenotype is extremely complex; for example, the effect of an allele often depends upon both the environment and the individual’s genetic background. To better understand these complex relationships, we examined the effects of four quantitative trait nucleotides (QTN) in three genes that cause variation in sporulation efficiency between vineyard and oak tree strains of yeast

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Summary

Introduction

As we identify more genetic loci that underlie complex traits, the challenge remains to understand and predict the effects of the causal genetic variants upon individuals’ phenotypes. The relationship between genotype and phenotype is rarely simple. The effect of an allele often depends upon the environment, resulting in gene-environment interactions (GxE). Gene-gene interactions take place that render the effect of one locus dependent upon the genotype at another locus. Genetic interactions can occur between characterized loci (epistasis) [6,7], or between one known locus and other unknown loci (genetic background effects) [8]. If individuals vary in their environmental exposure and genetic makeup, as they almost always do in nature, GxE and genetic interactions will create differences in the effects of alleles among individuals

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